Autophagy in maternal tissues contributes to Arabidopsis thaliana seed development

Seeds are an essential food source, providing nutrients for germination and early seedling growth. Degradation events in the seed and the mother plant accompany seed development. One degradation mechanism is autophagy, facilitating cellular component breakdown in the lytic organelle. Autophagy influences various aspects of plant physiology, specifically nutrient availability and remobilization, suggesting its involvement in source-sink interactions. During seed development, autophagy was shown to affect nutrient remobilization from mother plants and function in the embryo. Yet, these studies examined autophagy-knockout (atg mutant) plants, making it impossible to distinguish between the contribution of autophagy in the source (i.e., the mother plant) and the sink tissue (i.e., the embryo). To address this, we employed a novel approach to differentiate between autophagy in source and sink tissues. We investigated how autophagy in the maternal tissue affects seed development by performing reciprocal crosses between WT and atg mutant Arabidopsis thaliana plants. Although F1 seedlings possessed a functional autophagy mechanism, etiolated F1 plants from maternal atg mutants displayed reduced growth. This was attributed to altered protein but not lipid accumulation in the seeds, suggesting autophagy differentially regulates carbon and nitrogen remobilization. Surprisingly, F1 seeds of maternal atg mutants exhibited faster germination, resulting from different seed coat development. Our study emphasizes the significance of examining autophagy in a tissue-specific manner, revealing valuable insights into the interplay between different tissues during seed development. It sheds light on the tissue-specific functions of autophagy, offering potential for new research into the underlying mechanisms governing seed development and crop yield.

[1]  Heike Seybold,et al.  Metabolism and autophagy in plants—a perfect match , 2022, FEBS letters.

[2]  Yasin F. Dagdas,et al.  Autophagy promotes programmed cell death and corpse clearance in specific cell types of the Arabidopsis root cap , 2022, Current Biology.

[3]  Yuhai Cui,et al.  Endosperm–Embryo Communications: Recent Advances and Perspectives , 2021, Plants.

[4]  D. Bassham,et al.  Autophagy during drought: Function, regulation, and potential application. , 2021, The Plant journal : for cell and molecular biology.

[5]  W. Araújo,et al.  Autophagy is required for lipid homeostasis during dark-induced senescence. , 2021, Plant physiology.

[6]  R. Vierstra,et al.  Autophagy Plays Prominent Roles in Amino Acid, Nucleotide, and Carbohydrate Metabolism during Fixed-Carbon Starvation in Maize. , 2020, The Plant cell.

[7]  W. Araújo,et al.  Autophagy is required for lipid homeostasis during dark-induced senescence in Arabidopsis , 2020, bioRxiv.

[8]  R. Vierstra,et al.  Autophagy Plays Prominent Roles in Amino Acid, Nucleotide, and Carbohydrate Metabolism during Fixed-Carbon Starvation in Maize[OPEN] , 2020, Plant Cell.

[9]  Y. Brotman,et al.  Liquid Chromatography-Mass Spectrometry (LC-MS)-Based Analysis for Lipophilic Compound Profiling in Plants. , 2020, Current protocols in plant biology.

[10]  Wenyu Yang,et al.  A matter of life and death: molecular, physiological and environmental regulation of seed longevity. , 2019, Plant, cell & environment.

[11]  David S. Wishart,et al.  Using MetaboAnalyst 4.0 for Comprehensive and Integrative Metabolomics Data Analysis , 2019, Current protocols in bioinformatics.

[12]  Toshihiro Obata,et al.  Metabolic Dynamics of Developing Rice Seeds Under High Night-Time Temperature Stress , 2019, Front. Plant Sci..

[13]  Yasin F. Dagdas,et al.  Autophagy mediates temporary reprogramming and dedifferentiation in plant somatic cells , 2019, bioRxiv.

[14]  R. Vierstra,et al.  Maize multi-omics reveal roles for autophagic recycling in proteome remodelling and lipid turnover , 2018, Nature Plants.

[15]  T. Steinbrecher,et al.  Tissue and cellular mechanics of seeds. , 2018, Current opinion in genetics & development.

[16]  H. Ishida,et al.  Vacuolar Protein Degradation via Autophagy Provides Substrates to Amino Acid Catabolic Pathways as an Adaptive Response to Sugar Starvation in Arabidopsis thaliana , 2018, Plant & cell physiology.

[17]  A. Fernie,et al.  Next-generation strategies for understanding and influencing source-sink relations in crop plants. , 2018, Current opinion in plant biology.

[18]  R. Vierstra,et al.  Autophagy: The Master of Bulk and Selective Recycling. , 2018, Annual review of plant biology.

[19]  F. Baluška,et al.  Autophagy-related approaches for improving nutrient use efficiency and crop yield protection. , 2018, Journal of experimental botany.

[20]  C. Masclaux-Daubresse,et al.  Autophagy controls resource allocation and protein storage accumulation in Arabidopsis seeds , 2018, Journal of experimental botany.

[21]  K. Ljung,et al.  Transcriptional stimulation of rate-limiting components of the autophagic pathway improves plant fitness , 2018, Journal of experimental botany.

[22]  C. Masclaux-Daubresse,et al.  Source and sink mechanisms of nitrogen transport and use. , 2018, The New phytologist.

[23]  M. Audran,et al.  Liquid chromatography - high resolution mass spectrometry-based metabolomic approach for the detection of Continuous Erythropoiesis Receptor Activator effects in horse doping control. , 2017, Journal of chromatography. A.

[24]  Steven Penfield,et al.  Seed dormancy and germination , 2017, Current Biology.

[25]  A. Fernie,et al.  Autophagy Deficiency Compromises Alternative Pathways of Respiration following Energy Deprivation in Arabidopsis thaliana1 , 2017, Plant Physiology.

[26]  D. Sueldo,et al.  Plant life needs cell death, but does plant cell death need Cys proteases? , 2017, The FEBS journal.

[27]  Helen M. North,et al.  Sticking to cellulose: exploiting Arabidopsis seed coat mucilage to understand cellulose biosynthesis and cell wall polysaccharide interactions. , 2017, The New phytologist.

[28]  P. Giavalisco,et al.  Protocol: a fast, comprehensive and reproducible one-step extraction method for the rapid preparation of polar and semi-polar metabolites, lipids, proteins, starch and cell wall polymers from a single sample , 2016, Plant Methods.

[29]  B. Usadel,et al.  Extensive Natural Variation in Arabidopsis Seed Mucilage Structure , 2016, Front. Plant Sci..

[30]  Joshua S Yuan,et al.  Redesigning photosynthesis to sustainably meet global food and bioenergy demand , 2015, Proceedings of the National Academy of Sciences.

[31]  R. Vierstra,et al.  Autophagic Recycling Plays a Central Role in Maize Nitrogen Remobilization , 2015, Plant Cell.

[32]  A. Fernie,et al.  Global Analysis of the Role of Autophagy in Cellular Metabolism and Energy Homeostasis in Arabidopsis Seedlings under Carbon Starvation[OPEN] , 2015, Plant Cell.

[33]  A. Fernie,et al.  Liquid chromatography high-resolution mass spectrometry for fatty acid profiling. , 2015, The Plant journal : for cell and molecular biology.

[34]  A. Fernie,et al.  An update on source-to-sink carbon partitioning in tomato , 2014, Front. Plant Sci..

[35]  A. Fischer,et al.  Senescence, nutrient remobilization, and yield in wheat and barley. , 2014, Journal of experimental botany.

[36]  K. Shirasu,et al.  Stitching together the Multiple Dimensions of Autophagy Using Metabolomics and Transcriptomics Reveals Impacts on Metabolism, Development, and Plant Responses to the Environment in Arabidopsis[C][W] , 2014, Plant Cell.

[37]  Jie Zhou,et al.  Role and regulation of autophagy in heat stress responses of tomato plants , 2014, Front. Plant Sci..

[38]  Kazuki Saito,et al.  OsATG7 is required for autophagy-dependent lipid metabolism in rice postmeiotic anther development , 2014, Autophagy.

[39]  K. Shirasu,et al.  Organ-specific quality control of plant peroxisomes is mediated by autophagy , 2014, Journal of Cell Science.

[40]  Sollapura J. Vishwanath,et al.  Seed Coat Permeability Test: Tetrazolium Penetration Assay , 2014 .

[41]  F. Dédaldéchamp,et al.  Source-to-sink transport of sugar and regulation by environmental factors , 2013, Front. Plant Sci..

[42]  S. Ryter,et al.  Autophagy: A critical regulator of cellular metabolism and homeostasis , 2013, Molecules and cells.

[43]  Nese Sreenivasulu,et al.  Seed-development programs: a systems biology-based comparison between dicots and monocots. , 2013, Annual review of plant biology.

[44]  Kevin W Eliceiri,et al.  NIH Image to ImageJ: 25 years of image analysis , 2012, Nature Methods.

[45]  D. Bassham,et al.  Autophagy: pathways for self-eating in plant cells. , 2012, Annual review of plant biology.

[46]  Anne Guiboileau,et al.  Autophagy machinery controls nitrogen remobilization at the whole-plant level under both limiting and ample nitrate conditions in Arabidopsis. , 2012, The New phytologist.

[47]  G. Galili,et al.  Variations on a theme: plant autophagy in comparison to yeast and mammals , 2012, Protoplasma.

[48]  D. Lobell,et al.  Climate Trends and Global Crop Production Since 1980 , 2011, Science.

[49]  A. Marion-Poll,et al.  CESA5 Is Required for the Synthesis of Cellulose with a Role in Structuring the Adherent Mucilage of Arabidopsis Seeds1[C][W] , 2011, Plant Physiology.

[50]  G. Galili,et al.  Variations on a theme: plant autophagy in comparison to yeast and mammals , 2011, Protoplasma.

[51]  C. Lillo,et al.  From signal transduction to autophagy of plant cell organelles: lessons from yeast and mammals and plant-specific features , 2010, Protoplasma.

[52]  Y. Kamiya,et al.  Autophagy Negatively Regulates Cell Death by Controlling NPR1-Dependent Salicylic Acid Signaling during Senescence and the Innate Immune Response in Arabidopsis[W][OA] , 2009, The Plant Cell Online.

[53]  D. Bassham Function and regulation of macroautophagy in plants. , 2009, Biochimica et biophysica acta.

[54]  Jonathan D. G. Jones,et al.  Autophagic Components Contribute to Hypersensitive Cell Death in Arabidopsis , 2009, Cell.

[55]  R. Vierstra,et al.  The ATG Autophagic Conjugation System in Maize: ATG Transcripts and Abundance of the ATG8-Lipid Adduct Are Regulated by Development and Nutrient Availability1[W][OA] , 2008, Plant Physiology.

[56]  Sébastien Baud,et al.  Storage Reserve Accumulation in Arabidopsis: Metabolic and Developmental Control of Seed Filling , 2008, The arabidopsis book.

[57]  J. Ohlrogge,et al.  Identification of acyltransferases required for cutin biosynthesis and production of cutin with suberin-like monomers , 2007, Proceedings of the National Academy of Sciences.

[58]  James B. Hicks,et al.  A plant DNA minipreparation: Version II , 1983, Plant Molecular Biology Reporter.

[59]  K. Yoshimoto,et al.  Autophagy in Development and Stress Responses of Plants , 2006, Autophagy.

[60]  C. Benning,et al.  WRINKLED1 encodes an AP2/EREB domain protein involved in the control of storage compound biosynthesis in Arabidopsis. , 2004, The Plant journal : for cell and molecular biology.

[61]  R. Vierstra,et al.  The APG8/12-activating Enzyme APG7 Is Required for Proper Nutrient Recycling and Senescence in Arabidopsis thaliana * , 2002, The Journal of Biological Chemistry.

[62]  J. Görlach,et al.  Growth Stage–Based Phenotypic Analysis of Arabidopsis , 2001, The Plant Cell Online.

[63]  W. Willats,et al.  In-situ analysis of pectic polysaccharides in seed mucilage and at the root surface of Arabidopsis thaliana , 2001, Planta.

[64]  K. McCoy,et al.  The Biochemical and Cellular Basis of Cell Proliferation Assays That Use Tetrazolium Salts , 1996 .

[65]  G. Galili,et al.  Evidence for a novel route of wheat storage proteins to vacuoles , 1992, The Journal of cell biology.

[66]  J. Bamburg,et al.  A filter paper dye-binding assay for quantitative determination of protein without interference from reducing agents or detergents. , 1990, Analytical biochemistry.

[67]  S. Fling,et al.  Peptide and protein molecular weight determination by electrophoresis using a high-molarity tris buffer system without urea. , 1986, Analytical biochemistry.

[68]  H. Towbin,et al.  Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[69]  E. Werker,et al.  Relation Between the Anatomy of the Testa, Water Permeability and the Presence of Phenolics in the Genus Pisum , 1979 .

[70]  A. Mayer,et al.  Permeability of seed coats to water as related to drying conditions and metabolism of phenolics. , 1974, Plant physiology.

[71]  W. Clark A matter of "will". , 1971 .

[72]  U. K. Laemmli,et al.  Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4 , 1970, Nature.

[73]  M. E. Mace Histochemical Localization of Phenols in Healthy and Diseased Banana Roots , 1963 .